3D chromatin maps of a brown alga reveal U/V sex chromosome spatial organization

• Published in: Nature communications 2024-11, Vol.15 (1), p.9590-15, Article 9590
• Main Authors: Liu, Pengfei, Vigneau, Jeromine, Craig, Rory J., Barrera-Redondo, Josué, Avdievich, Elena, Martinho, Claudia, Borg, Michael, Haas, Fabian B., Liu, Chang, Coelho, Susana M.
• Format: Article
• Language: English
• Subjects: 45; 45/15; 45/23; 45/77; 45/90; 631/208/182; 631/208/212; 631/208/726; 64; Algae; Centromere - genetics; Centromere - metabolism; Centromeres; Chromatin; Chromatin - genetics; Chromatin - metabolism; Chromosome 6; Chromosome Mapping; Chromosomes; Dynamic structural analysis; Ectocarpus; Folding; Gene expression; Gene mapping; Genomes; Histones; Histones - genetics; Histones - metabolism; Humanities and Social Sciences; multidisciplinary; Phaeophyceae - genetics; Phaeophyceae - metabolism; Post-translation; Retroelements - genetics; Science; Science (multidisciplinary); Sex; Sex chromosomes; Sex Chromosomes - genetics; Sex determination; Telomere - genetics; Telomere - metabolism; Telomeres
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-53453-5

Nuclear three dimensional (3D) folding of chromatin structure has been linked to gene expression regulation and correct developmental programs, but little is known about the 3D architecture of sex chromosomes within the nucleus, and how that impacts their role in sex determination. Here, we determine the sex-specific 3D organization of the model brown alga Ectocarpus chromosomes at 2 kb resolution, by mapping long-range chromosomal interactions using Hi-C coupled with Oxford Nanopore long reads. We report that Ectocarpus interphase chromatin exhibits a non-Rabl conformation, with strong contacts among telomeres and among centromeres, which feature centromere-specific LTR retrotransposons. The Ectocarpus chromosomes do not contain large local interactive domains that resemble TADs described in animals, but their 3D genome organization is largely shaped by post-translational modifications of histone proteins. We show that the sex determining region (SDR) within the U and V chromosomes are insulated and span the centromeres and we link sex-specific chromatin dynamics and gene expression levels to the 3D chromatin structure of the U and V chromosomes. Finally, we uncover the unique conformation of a large genomic region on chromosome 6 harboring an endogenous viral element, providing insights regarding the impact of a latent giant dsDNA virus on the host genome’s 3D chromosomal folding. The 3D chromatin organisation of sex chromosomes within the nucleus remains elusive. This study determines the chromatin architecture of the brown alga Ectocarpus , linking sex-specific chromatin dynamics, histone modification and gene expression to the 3D structure of the U and V sex chromosomes.